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Light-dependent plasticity of the morphology of horizontal cell terminals in cone pedicles of fish retinas

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Journal of Neurocytology

Summary

Horizontal cell terminals lateral to the synaptic ribbons in goldfish cone pedicles give rise to 0.3 μm long, finger-like extensions in the light-adapted state. These structures, called spinules, disappear almost completely after dark adaptation. The ultrastructure of the horizontal cell terminals is characterized by the presence of occasional microtubules, microfilaments and sparse irregular vesicles; in the dark, large multivesicular bodies can also be found. Two types of membrane densities are described in the horizontal cell terminals, one of which is typically located at the tip of the spinules. Their positive reaction to E-PTA makes it probable that the spinules are synaptic structures. Reconstruction of serial sections shows about 12 spinules per terminal in the light but only two in the dark. Formation and disappearance of the spinules takes about 60 min and involves a transitional stage in the form of a spherical structure. Spinules can be found in five other teleost species, with a darkness-induced reduction in number, but not in the horizontal cell terminals of the mudpuppy, turtle and mammals.

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References

  • Ali, M. A. (1959) The ocular structure, retinomotor and photobehavioral responses of juvenile pacific salmon.Canadian Journal of Zoology 37, 965–96.

    Google Scholar 

  • Bailey, C. H., Thompson, E. B., Castellucci, V. F. &Kandel, E. R. (1979) Ultrastructure of the synapses of sensory neurons that mediate the gill-withdrawal reflex inAplysia.Journal of Neurocytology 8, 415–44.

    Google Scholar 

  • Basinger, S., Hoffman, R. &Matthes, M. (1976) Photoreceptor shedding is initiated by light in the frog retina.Science 194, 1074–6.

    Google Scholar 

  • Besharse, J. C., Hollyfield, J. G. &Rayborn, M. E. (1977) Turnover of rod photoreceptor outer segments. II. Membrane addition and loss in relationship to light.Journal of Cell Biology 75, 507–27.

    Google Scholar 

  • Bloom, F. E. &Aghajanian, G. K. (1968) Fine structural and cytochemical analysis of the staining of synaptic junctions with phosphotungstic acid.Journal of Ultrastructure Research 22, 361–75.

    Google Scholar 

  • Cervetto, L. &Fuortes, M. G. F. (1978) Excitation and interaction in the retina.Annual Review of Biophysics and Bioengineering 7, 229–51.

    Google Scholar 

  • Coss, R. G. &Globus, A. (1978) Spine stems on tectal interneurons in jewel fish are shortened by social stimulation.Science 200, 787–90.

    Google Scholar 

  • Cragg, B. G. (1972) Plasticity of synapses. InThe Structure and Function of Nervous Tissue (edited byBourne, G. H.), Vol. IV, pp. 1–60. New York: Academic Press.

    Google Scholar 

  • Dowling, J. E., Ehinger, B. &Hedden, W. L. (1976) The interplexiform cell: A new type of retinal neuron.Investigative Ophthalmology and Visual Science 15, 916–26.

    Google Scholar 

  • Dowling, J. E. (1979) A new retinal neurone-the interplexiform cell.Trends in Neuro Sciences 2, 189–91.

    Google Scholar 

  • Gallego, A. (1976) Comparative study of the horizontal cells in the vertebrate retina: mammals and birds. InNeural Principles in Vision (edited byZettler, F. andWeiler, R.), pp. 26–62. Berlin, Heidelberg, New York: Springer-Verlag.

    Google Scholar 

  • Gerschenfeld, H. M. &Piccolino, M. (1977) Muscarinic antagonists block cone to horizontal cell transmission in turtle retina.Nature 268, 257–9.

    Google Scholar 

  • Gray, E. G. (1963) Electron microscopy of presynaptic organelles in the spinal cord.Journal of Anatomy 97, 101–6.

    Google Scholar 

  • Hamlyn, L. H. (1963) The fine structure of the mossy fibre endings in the hippocampus of the rabbit.Journal of Anatomy 96, 112–20.

    Google Scholar 

  • Hollyfield, J. G. &Basinger, S. F. (1978) Photoreceptor shedding can be initiated within the eye.Nature 274, 794–6.

    Google Scholar 

  • Hollyfield, J. G., Besharse, J. C. &Rayborn, M. E. (1977) Turnover of rod photoreceptor outer segments. I. Membrane addition and loss in relationship to temperature.Journal of Cell Biology 75, 490–506.

    Google Scholar 

  • Kaneko, A. (1979) Physiology of the retina.Annual Review of Neuroscience 2, 169–91.

    Google Scholar 

  • Karnovsky, M. J. (1965) A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy.Journal of Cell Biology 27, 137A.

    Google Scholar 

  • Kolb, H. &West, R. W. (1977) Synaptic connections of the interplexiform cell in the retina of the cat.Journal of Neurocytology 6, 155–70.

    Google Scholar 

  • Marc, R. E., Stell, W. K., Bok, D. &Lam, D. M. K. (1978) GABA-ergic pathways in the goldfish retina.Journal of Comparative Neurology 182, 221–46.

    Google Scholar 

  • Monaghan, P. &Osborne, M. P. (1975) Light-induced formation of dense core vesicles in rod photoreceptors in retinas ofXenopus laevis.Nature 257, 586–7.

    Google Scholar 

  • Mountford, S. (1963) Effects of light and dark adaptation on the vesicle population of receptor-bipolar synapses.Journal of Ultrastructure Research 9, 403–19.

    Google Scholar 

  • O'day, W. T. &Young, R. W. (1978) Rhythmic daily shedding of outer-segment membranes by visual cells in the goldfish.Journal of Cell Biology 76, 593–604.

    Google Scholar 

  • Osborne, M. P. &Monaghan, P. (1976) Effects of light and dark upon photoreceptor synapses in the retina ofXenopus laevis.Cell and Tissue Research 173, 211–20.

    Google Scholar 

  • Peters, A., Palay, S. L. &Webster, H. deF. (1976)The Fine Structure of the Nervous System: The neurons and supporting cells. Philadelphia: Saunders.

    Google Scholar 

  • Pfenninger, K. H. (1973) Synaptic morphology and cytochemistry.Progress in Histochemistry and Cytochemistry 5, 1–86.

    Google Scholar 

  • Raynauld, J. P., Laviolette, J. R. &Wagner, H.-J. (1979) Goldfish retina: a correlate between cone activity and morphology of the horizontal cell in cone pedicles.Science 204, 1436–8.

    Google Scholar 

  • Schaeffer, S. F. &Raviola, E. (1976) Ultrastructural analysis of functional changes in the synaptic endings of turtle cone cells.Cold Spring Harbor Symposia on Quantitative Biology 40, 521–8.

    Google Scholar 

  • Schaeffer, S. F. &Raviola, E. (1978) Membrane recycling in the cone cell endings of the turtle retina.Journal of Cell Biology 79, 802–25.

    Google Scholar 

  • Scholes, J. H. (1975) Colour receptors, and their synaptic connexions in the retina of a cyprinid fish.Philosophical Transactions of the Royal Society of London, Series B 270, 61–118.

    Google Scholar 

  • Schwartz, I. R. &Bok, D. (1979) Electron microscopic localization of [125I]α-bungarotoxin binding sites in the outer plexiform layer of the goldfish retina.Journal of Neurocytology 8, 53–66.

    Google Scholar 

  • Stell, W. K. (1966)The structure of horizontal cells and synaptic relations in the outer plexiform layer of the goldfish retina, as revealed by the Golgi method and electron microscopy. Thesis, Faculty of Biological Science, University of Chicago.

  • Stell, W. K. (1975) Horizontal cell axons and axon terminals in goldfish retina.Journal of Comparative Neurology 159, 503–20.

    Google Scholar 

  • Stell, W. K. (1976) Functional polarization of horizontal cell dendrites in goldfish retina.Investigative Ophthalmology and Visual Science 15, 895–908.

    Google Scholar 

  • Stell, W. K. &Harosi, F. (1976) Cone structure and visual pigment content in the retina of the goldfish.Vision Research 16, 647–57.

    Google Scholar 

  • Stell, W. K. &Lightfoot, D. O. (1975) Color-specific interconnections of cones and horizontal cells in the retina of the goldfish.Journal of Comparative Neurology 159, 473–502.

    Google Scholar 

  • Stell, W. K., Lightfoot, D. O. &Wheeler, T. G. (1975) Goldfish retina: Functional polarization of cone horizontal cell dendrites and synapses.Science 190, 989–90.

    Google Scholar 

  • Wagner, H.-J. (1975) Quantitative changes of synaptic ribbons in the cone pedicles ofNannacara: Light dependent or governed by a circadian rhythm? InVision in Fishes: New Approaches in Research (edited byAli, M. A.), pp. 679–86. New York, London: Plenum Press.

    Google Scholar 

  • Wagner, H.-J. (1978) Cell types and connectivity patterns in mosaic retinas.Advances in Anatomy, Embryology and Cell Biology 55, 3.

    Google Scholar 

  • Wagner, H.-J. &Ali, M. A. (1977) Cone synaptic ribbons and retinomotor changes in the brook trout,Salvelinus fontinalis (Salmonidae, Teleostei), under various experimental conditions.Canadian Journal of Zoology 55, 1684–91.

    Google Scholar 

  • Werblin, F. S. &Dowling, J. E. (1969) Organization of the retina of the mudpuppy,Necturus maculosus. II. Intracellular recording.Journal of Neurophysiology 32, 339–55.

    Google Scholar 

  • Wu, S. M. &Dowling, J. E. (1978) L-Aspartate: Evidence for a role in cone photoreceptor synaptic transmission in the carp retina.Proceedings of the National Academy of Science (U.S.A.) 75, 5205–9.

    Google Scholar 

  • Young, R. W. (1967) The renewal of photoreceptor outer segments.Journal of Cell Biology 33, 61–72.

    Google Scholar 

  • Young, R. W. (1977) The daily rhythm of shedding and degradation of cone outer segment membranes in the lizard retina.Journal of Ultrastructure Research 61, 172–85.

    Google Scholar 

  • Young, R. W. (1978) Rhythmic shedding of rod and cone membranes.Investigative Ophthalmology and Visual Science 17, 105–16.

    Google Scholar 

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The morphological changes reported in this paper were first observed in the laboratory of Professor J. P. Raynauld at the Université de Montréal and presented in a preliminary form in Science (Raynauldet al., 1979) and at the 1979 ARVO Meeting.

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Wagner, H.J. Light-dependent plasticity of the morphology of horizontal cell terminals in cone pedicles of fish retinas. J Neurocytol 9, 573–590 (1980). https://doi.org/10.1007/BF01205026

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  • DOI: https://doi.org/10.1007/BF01205026

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